Prosopis pods as human food, with special reference to Kenya#

SK Choge1, NM Pasiecznik2, M Harvey3, J Wright3, SZ Awan3 and PJC Harris4* 1 Kenya Forestry Research Institute, P.O. Box 20412, 00200 Nairobi, Kenya 2 Agroforestry Enterprises, Villebeuf, 71550 Cussy-en-Morvan, France 3 Henry Doubleday Research Association, Ryton Organic Gardens, Coventry CV8 3LG, UK 4 Department of Geography, Environment and Disaster Management, Coventry University, Priory Street, Coventry CV1 5FB, UK

Abstract

Several and shrub species of the genus from South and Central America have been distributed around the dry regions of the world over the past 200 years. The first documented introduction of Prosopisn i Kenya was in 1973, since when it has spread widely, adversely affecting natural habitats, rangelands and cultivated areas. P.s juliflora i the most common naturalised species in Kenya, but P. pallida also occurs. In contrast to their undesirable effects as invasive weeds, many Prosopis species are valuable multipurpose resources in their native range, providing timber, firewood, live- stock feed, human food, shade, shelter and soil improvement. The pods, which are high in sugars, carbohydrates and protein, have been a historic source of food for human populations in North and South America providing flour and other edible products. However, this indigenous knowledge has not followed the Prosopis and the fruit are unused or provide only fodder for livestock in most of Africa and Asia. Although Prosopis will not easily be eradicated in Kenya, a degree of control may be achieved through intensive utilisation of tree products and by improved management. In 2005, a project was launched in Kenya to develop income-generating activities using Prosopis. A workshop in 2006 explored the possibility of producing locally-acceptable food from Prosopis flour. Taste tests and feedback on the different recipes indicated that all of the food made with 20% Prosopis flour had a pleasant taste. Preliminary analyses of Prosopis flour samples from Kenya indicate good nutritional properties, but also the presence of aflatoxins and Ochratoxin A. Further study is required to determine toxin levels in freshly harvested pods, and in pods and flour after various periods of storage, and to develop appropriate harvesting and storage methods to maximise nutritional benefit and minimise risk to human health.

Keywords: Aflatoxin, human food, Kenya, Ochratoxin A, Prosopis

Introduction commercial suppliers without reference to origin or quality (Johansson, 1990; Otsamo and Maua, 1993). Over the years, Prosopis has spread outside the designated plantation areas, The genus Prosopisn i the family Leguminosae (, ) adversely affecting natural habitats, rangelands and cultivated subfamily is native to the Americas, Africa and areas in many parts of the country (Choge et al., 2002). P. juli- Asia, and comprises 44 species (Burkart, 1976). Prosopis spe- floras i the most common naturalised species but P. pallida has cies are generally fast-growing, drought-resistant, nitrogen- also been confirmed by the present authors.Prosopis has been fixing trees or shrubs adapted to poor and saline soils in arid declared a noxious weed in Kenya, with legal disputes over and semi-arid zones. Several species from South and Central compensation for its spread and subsequent loss of liveli- America, especially the sub-tropical P. chilensis, P. glandulosa hoods, especially in pastoral regions. and P. velutina, and the tropical P. juliflora and P. pallida, have In contrast to their undesirable effects as invasive weeds, been distributed around the world over the last 200 years and many Prosopis species are valuable multipurpose resources in are now widespread in dry parts of Sahelian and East Africa, their native range, providing timber, firewood, livestock feed, South Africa, Pakistan, India, Brazil and Australia (Pasiecznik human food, shade, shelter and soil improvement (Pasiecznik et al., 2001). et al., 2001). This paper reviews the extensive scientific litera- The earliest known introductions of oProsopis t Africa were ture on the uses of Prosopiss a human food. Also presented are to Senegal (1822), South Africa (1880) and Egypt (1900) (Zim- the results of a project launched in Kenya to develop income- merman, 1991; Pasiecznik et al., 2001). In Kenya, the first docu- generating activities using Prosopis. Analysis of Prosopis pod mented introduction of Prosopis, from Brazil and Hawaii, was flour from Kenya was undertaken to assess the food quality in 1973 for rehabilitation of quarries near Mombassa (Johans- and safety of locally prepared material. A workshop in Kenya son, 1990). During the 1970s and early 1980s, there were unco- in 2006 explored the possibility of producing locally acceptable ordinated introductions of Prosopiso t many parts of Kenya by food from Prosopis flour. NGOs and government departments with sourced from Prosopis as human food

# Revised version. Originally presented at the International Sympo- -1 -1 sium on the Nutritional Value and Water Use of Indigenous Crops Pod yields as high as 100 kg·yr , and often 20 to 50 kg·yr for Improved Livelihoods held on 19 and 20 September 2006 at the have been recorded for single trees. If cultivated as an orchard University of Pretoria in Pretoria, South Africa crop, production is highly variable, normally ranging from 1 to * To whom all correspondence should be addressed. 8 t·ha-1·yr-1, but Prosopis can yield up to 10 t·ha-1 of fruit (Felker,  +44 24 7688 8483; fax: +44 24 7688 8400; 1979). The pods have been an historic source of food for human e-mail: [email protected] populations, for example in the Sonoran Desert in North Amer-

Available on website http://www.wrc.org.za 419 ISSN 0378-4738 = Water SA Vol. 33 No. 3 (Special Edition) 2007 ISSN 1816-7950 = Water SA (on-line) ica, where Indian tribes made flour and dough with the dried der substitute. Coffee substitute has been made from P. juliflora or toasted pulp from ripe pods (Simpson, 1977). In Northern in Brazil (Azevedo Rocha, 1987). Argentina, flour made from the pulp of sProsopis i known as ‘patay’ and is still consumed today (Ochoa, 1996). In , P. Nutritional qualities pallida pods are ground into flour to make bread, cakes or a rich porridge. Traditionally, dried pods were pounded in a The fruit produced by Prosopiss i high in sugars, carbohydrates pestle and mortar to produce a coarse flour, or ground using a and protein. Pods from species of section Algarobia of the genus, variety of stone mills (Felger, 1977). Other methods of manual which includes the common weedy species in Africa, contain or mechanical grinding have also proved successful for process- 7 to 22% protein, 30 to 75% carbohydrates, 11 to 35% crude fibre, ing Prosopis pods (Meyer et al., 1982; Saunders et al., 1986; 1 to 6% fat and 3 to 6% ash (e.g. Oduol et al., 1986; Galera et al., Del Valle et al., 1987; Grados and Cruz, 1996). The absence of 1992; Anttila et al., 1993). Care should be taken in interpreting starch is a limitation to Prosopis flour levels in bread formula- food value data for Prosopis from the literature as these may be tions. Mixing 5-25% Prosopis flour with wheat flour produces given for whole pods, or for only the pulp (mesocarp) or seed products which have acceptable taste. Sweet bread containing fractions. Table 1 shows the proximate analyses of whole pods 5% P. pallida flour is acceptable in texture and taste, though up of P. juliflora and P. pallida, the two species introduced into to 25% has been used in making biscuits, which also reduces the Kenya. amount of additional sugar required (Cruz, 1999). Further analyses of P. pallida fruit, but for pulp only, are Flour is the main product considered in this paper, but shown in Tables 2, 3 and 4. The main soluble component of the Prosopis pods also yield an impressive range of other food pulp of sP. pallida i sucrose (46%), representing over 90% of products. In Peru, pods of P. pallida are boiled into syrup total soluble sugars, while the reducing sugars, glucose, fructose called ‘algarrobina’. Another food product from Prosopiss i and xylose, are present in very small amounts (Cruz et al., 1987; ‘yupisín’, a beverage which is obtained by water extraction of Sáenz et al., 1987). Talpada (1985) found that the sugar content the sugars from the pod. A fermented beverage, ‘aloja’ can be of P. juliflora pods varied from 13 to 20% in different seasons produced and is used as a substitute for beer or wine (Cruz, and years, showing a strong environmental effect on pod com- 1986; Ochoa, 1996). In Brazil, the production of a protein isolate position. Soluble sugars from the pericarp of P. juliflora from (Baião et al., 1987) and a protein-enriched flour (Ruiz, 1997) Ecuador comprise 75% sucrose, 12% fructose, 5% glucose, 5% from P. juliflora and its application in bread-making have inositol and 1% raffinose (Marangoni and Alli, 1988). been reported. P. pallida pulp flour can also be used as an ingre- Dietary fibre represents 30% of the pulp and is largely dient in many other food preparations, such as cakes, ice creams insoluble. More than half of the fibre fraction consists of neutral and other desserts. P. pallida pulp flour has been converted into polysaccharides (Bravo et al., 1994). High iron levels have been an instantly soluble powder, and could be used as a cocoa pow- reported in P. juliflora from Ecuador and Brazil (Figueiredo,

TABLE 1 Proximate analysis of whole P. juliflora (PJ) and P. pallida (PP) pods (%) Species Location Dry matter Crude Crude fibre Ether Ash Nitrogen Source protein extract free extract PP Peru 85.9 9.1 18.4 1.0 3.9 65.3 a PJ Peru 82.0 9.1 13.6 0.4 5.8 71.1 a PP Brazil - 8.1 22.1 1.3 5.0 64.0 b PJ Brazil 87.4 7.1 12.3 1.1 3.3 63.6 c PJ India 88.5 12.3 28.0 1.3 1.4 46.3 d PJ Mexico 90.1 16.2 23.4 3.5 6.0 50.9 a PJ Niger 92.6 12.9 18.0 4.0 4.5 58.9 e PJ Kenya - 16.0 22.0 3.4 4.5 54.1 f PJ S. Africa - 13.9 27.7 3.0 4.8 50.6 g From: a - Díaz Celis (1995); b - Lima (1994); c - Galera et al. (1992); d – Anon. (1943); e - Touzeau (1973); f - Anttila et al. (1993); g - Gohl (1981).

TABLE 3 Mineral and vitamin composition of pulp from TABLE 2 P. pallida pods Composition of P. pallida pulp Minerals (g/kg dry Vitamins (mg/kg Component (g/100 g dry matter) matter) sample) Total soluble sugars 48.5 Potassium 26.5 Vitamin A not detected Total dietary fibre 32.2 Sodium1.1 Vitamin E 5 Protein (N x 6.25) 8.1 Calcium 0.8 Vitamin B1 1.9 Fat 0.8 Magnesium 0.9 Vitamin B2 0.6 Ash 3.6 Copper Trace Vitamin B6 2.35 Adapted from: Cruz et al. (1987); Cruz (1990); Saura Zinc Trace Nicotinic acid 31 et al. (1991); Salazar (1993); Bravo et al. (1994) ; Manganese Trace Vitamin C 60 Grados and Cruz (1996). Iron 0.3 Folic acid 0.18 Calcium pantothenate 10.5 From: Cruz et al. (1987).

420 Available on website http://www.wrc.org.za ISSN 0378-4738 = Water SA Vol. 33 No. 3 (Special Edition) 2007 ISSN 1816-7950 = Water SA (on-line) TABLE 4 TABLE 5 Amino acid composition of P. pallida pulp Composition of flour from whole pods of Amino acid (g/100 g dry Amino acid (g/100 g dry P. juliflora from Baringo District, Kenya matter) matter) Component (value/100 g Aspartic acid 8.51 Isoleucine 3.26 dry matter) Throenine 4.68 Leucine 7.94 Protein (g) 16.2 Serine 4.96 Tyrosine 2.84 Total sugars (g) 13.0 Glutamic acid 10.07 Phenylalanine 2.98 Fructose (g) 3.2 Proline 23.40 Lysine 4.26 Glucose (g) 0.8 Glycine 4.68 Histidine 1.99 Galactose (g) 0.8 Alanine 4.26 Arginine 4.82 Sucrose (g) 7.5 Cysteine 0.43 Tryptophan 0.89 Maltose (g) <0.4 Methionine 0.57 Hydroxyproline 2.13 Lactose (g) 0.7 Valine 7.80 Carbohydrate (g) 69.2 From: Cruz et al. (1987). Energy value (kJ) 1530 Dietary fibre (g) 47.8 1975; Marangoni and Alli, 1988) but no figures for its bio-avail- Fat (g) 2.12 ability are given. The vitamins C, B6 and calcium pantothenate Monosaturated fatty acids (g) 0.4 are present in significant amounts in pulp from P. pallida pods (Grados and Cruz, 1996). Polyunsaturated fatty acids (g) 1.06 Nearly all the essential amino acids are present in amounts Saturated fatty acids (g) 0.56 which fulfil the requirements of the FAO/WHO ‘standard Sodium (mg) 20 protein’, thus indicating an acceptable nutritional quality of Ash (g) 6.0 the protein. Methionine and cysteine are the limiting amino Total solids (g) 93.5 acids. The fat content of pulp is low (Table 2), but is reported to be 7% in P. pallida seed cotyledons (Jiménez and Vergara in the native range in South and Central America, this indig- 1977) with the major fatty acids found in extracted oil being enous knowledge has not followed Prosopis trees across the linoleic acid (39%), oleic acid (29%), palmitic acid (13%) Atlantic, where the fruits are unused or provide only fod- and stearic acid (10%). Similar values have been reported for der for livestock. Pasiecznik (2002) argues that in Central and P. juliflora (Marangoni and Alli, 1988). Table 5 shows the com- South America, many rural economies rely heavily on native position of flour from whole P. juliflora pods produced in the oProsopis t supply a trade in processed products, while this is course of the present study. This confirms the product as a high not the case where it was introduced. Thus, one reason why it protein, high sugar material of considerable human food value. often becomes an invasive weed, is because the full range of its uses and management is not known. Food safety Although Prosopis will not easily be eradicated in Kenya, a degree of control may be achieved through intensive utilisation Consumption of Prosopis products by humans, even as a staple of tree products and by improved management. Trading of its food, has not resulted in any recorded harmful effects on health products, converting a weed into a valuable resource, presents (Pasiecznik et al., 2001). Both Pak et al . (1977) with P. tama- an opportunity for socio-economic benefits to the communi- rugo and Becker and Grosjean (1980) with P. glandulosa and ties living in marginal areas of the country where extensive P. velutina failed to detect cyanogenic glycosides, but the latter areas of Prosopis are found. Furthermore, invasive Prosopis authors did find phytohaemaglutinins in the seeds which meant is now common in many of the parts of Sahelian and eastern they had to be heated (cooked) to eliminate this. Significantly Africa, including Kenya and Niger where large populations smaller amounts of polyphenols and tannins were found in pods face malnutrition due to drought, a situation exacerbated of P. pallida fruit than in (Ceratonia siliqua) pods (Salazar by mass movements of refugees in response to food short- 1993; Bravo et al. , 1994). Prosopis pods and seeds have been ages and military conflicts. In these situations Prosopis has reported to be almost totally devoid of trypsin inhibitor activity potential at least as a famine food, if not as a regular source (< 6 TIU/mg) (Zolfaghari and Harden, 1982; Ortega-Nieblas et of nutrition. al., 1996), although a trypsin inhibitor from P. juliflora seeds has been characterised (Monte-Negreiros et al., 1991). Hexanal, Developing Prosopis as a human food in Kenya which is an indicator of rancidity from oxidation of fats, was found in whole ground Prosopis seeds while mesocarp flour was Village-level trials devoid of this compound (Felker, pers. comm.). Prosopis flour from Argentina has been found to be free of aflatoxins (Felker, In 2005, a project was launched in Kenya to develop income- pers. comm.). In contrast, pods of Prosopis spp. in the wild in generating activities using Prosopis. This project is work- the Sonoran Desert in Arizona, USA, have been reported to have ing with villages in the Baringo District, which was selected high levels of aflatoxin and to be important reservoirs of afla- because of the problem with invasive Prosopis, its dry bushland toxin-producing fungi (Boyd and Cotty, 2001). Insect damaged ecology and low agricultural potential, high levels of poverty, pods had significantly higher aflatoxin than intact pods. good communication facilities, and proximity to urban markets. P. juliflora was introduced to the area in 1982 and has spread From weed to resource considerably. The first phase of the project was a workshop in Marigat Although food products made from Prosopis flour are consumed village in February 2006. The aim of the workshop was to

Available on website http://www.wrc.org.za 421 ISSN 0378-4738 = Water SA Vol. 33 No. 3 (Special Edition) 2007 ISSN 1816-7950 = Water SA (on-line) demonstrate and discuss Prosopis management and utilisation TABLE 6 methods including its use as human food. The workshop ran Analysis of flour# over four days with twenty-six trainees and a further ten partici- produced in Kenya pants including village chiefs, district officials and farmer field Analysis Level school facilitators. detected (µg∙kg-1) In Baringo District, the common types of flour used are Ochratoxin A 38.0 maize, wheat and occasionally millet. Wheat flour is used for Total aflatoxin 5.8 chapattis, pancakes, mandazi and cakes, and maize flour for the Aflatoxin B1 4.7 traditional ugali and uji. For mandazi, it was noted, a propor- # tion of wheat flour can be substituted with maize flour, being Flour produced from whole pods harvested cheaper, to reduce the cost with no real effect on taste. This was from wild trees and milled into flour taken as an example of how P. juliflora flour could be used as a low-cost and nutritious substitute for up to a quarter of the flour and Rasmussen, 2005). Similarly, significant levels of aflatoxin in traditional recipes. in common food products have been routinely reported in West A tractor-powered hammer mill was used to mill whole Africa (Bankole and Adebanjo, 2003) and East Africa (Kaaya pods, including seeds, into coarse flour. This was milled again in and Warren, 2005). In Uganda 29.6% of common food samples a local common roller mill (‘pasha’) for finer flour, but was still analysed tested positive for aflatoxin and approximately 12% considered unsuitable and was passed through a still finer sieve. exceeded 100 ppm total aflatoxin (Kaaya and Warren, 2005). Flour from whole machine-milled pods that include seeds Nevertheless, the results in Table 6 are of sufficient concern was preferred in terms of taste to that from pestle and mor- to warrant further study to determine toxin levels in freshly tar ground pods with seeds and capsules removed. Including harvested pods, and in pods and flour after various periods seeds will increase the protein content and reduce the bitter- of storage, and to develop appropriate harvesting and stor- ness. Pods from P. pallida are known to be sweeter, but are age methods to minimise risk to human health. Among steps relatively rare in Kenya. that may be necessary are early harvest, thorough drying and After demonstration by a trainer using a mixture of wheat control of moisture levels during storage, discarding infested flour with 20% finely sievedProsopis flour, the participants made seeds, control of insect infestation and avoidance of carry over chapattis at different mix ratios, pancakes, mandazi, ugali, uji of inoculum in storage facilities. and cake, and were proactive in developing new recipes, which Some indications of appropriate methods can be found are now available as a booklet. All of the food was cooked on in the traditional and improved storage and handling meth- traditional stoves using Prosopis charcoal. Taste tests and feed- ods used in South America. Traditional pod stores in North back on the different recipes indicated that all of the food America tended to consist of large baskets made from natural made with 20% Prosopis flour had a pleasant taste, whereas fibres, with a rain-proof roof, raised off the ground to prevent ugali made with 40% flour was not liked. Outreach strate- predation and to keep the pods dry (Felger, 1977). In Bra- gies to spread the knowledge further are to include cookery zil, standard agricultural barns used for storing other dried demonstrations, samples and photos at public functions, and animal feeds or special rooms with wooden floors and walls church and women’s groups, and promotion of the recipes in are used (e.g. Da Silva, 1996). In Peru, rustic closed rooms the media and in a local hotel. were used, made from mud bricks. These have largely been replaced with built block buildings (Grados and Cruz, 1996). Analysis of food quality and safety Special storage units for P. pallida pods are built, 5 x 5 x 4 m high, which are capable of storing 40 t of pods (Díaz Celis, Clearly, if Prosopiss i to be adopted as a human food in Kenya 1995). In India, layers of dry pods are laid down alternately as is already the case in South America, then it will be necessary with layers of sand. This is said to increase storage time to to confirm the nutritional value of the product and to test it for three years. Periodic checking of the pods in the store is rec- microbial contamination, mycotoxins and antinutritional fac- ommended to assess any damage due to fungal infections, tors. A sample of flour from Kenya was tested for aflatoxins and high moisture or pests. Removal of infected pods should be Ochratoxin A by Leatherhead Food International, Leatherhead, carried out immediately. In Peru, however, once a pod store is UK. The results in Table 6 indicate the presencce of aflatoxins filled, it is sealed with clay and opened only when the entire and Ochratoxin A in the Prosopis flour. The levels of total afla- batch is to be sold. toxin and Aflatoxin B1 exceed the stringent EU maximum levels for cereals of 5 and 3 µg∙kg-1, respectively, but not the maximum Further work levels adopted in the USA (10 µg∙kg-1), Brazil (20 µg∙kg-1) or India (30 µg∙kg-1) (FAO, 2004). The Ochratoxin A level in Prosopis To further disseminate the findings of the study, women from Bar- flour exceeded the maximum level of 5 µg∙kg-1 that has been pro- ingo District ran a Prosopis cookery demonstration day at KEFRI posed as an international standard by CODEX for Ochratoxin A in Nairobi. Plans are in progress to introduce the idea to other in wheat, barley, rye and their derived products (USFDA, 2003), drought-affected areas of Kenya. Further work is required on: though this standard was opposed by some countries such as • Milling, capacity for crushing the seeds, and accessibility India who argued for a maximum level of 20 µg∙kg-1. and cost to pod collectors However, only one Kenyan Prosopis flour sample has been • Pod collection methods, drying time and methods and stor- analysed so far and this had been produced from pods harvested age for preserving flour quality and pest control in the wild and stored for several months. Levels of Ochratoxin • Different recipes and preparation methods for flour products A far higher than the levels shown in Table 6 are occasion- • Nutritional composition of the flour, and different ratios of ally found in samples, including in European grain samples, Prosopis to other flours when harvest, drying and storage conditions favour fungal • The potential for local production of other food products growth and toxin production (Jørgensen et al., 1996; Elmholt from Prosopis pods.

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